Neuroglial interactions underpinning myelin plasticity

The CNS is extremely responsive to an ever‐changing environment. Studies of neural circuit plasticity focus almost exclusively on functional and structural changes of neuronal synapses. In recent years, however, myelin plasticity has emerged as a potential modulator of neuronal networks. Myelination of previously unmyelinated axons and changes in the structure of myelin on already‐myelinated axons (similar to changes in internode number and length or myelin thickness or geometry of the nodal area) can in theory have significant effects on the function of neuronal networks. In this article, the authors review the current evidence for myelin changes occurring in the adult CNS, highlight some potential underlying mechanisms of how neuronal activity may regulate myelin changes, and explore the similarities between neuronal and myelin plasticity. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 78: 93–107, 2018

[1]  Jeffrey A. Loeb,et al.  Neuregulin-1 Type III Determines the Ensheathment Fate of Axons , 2005, Neuron.

[2]  R. Fern,et al.  Neurotransmitter signaling in white matter , 2014, Glia.

[3]  M. A. Matthews,et al.  A quantitative study of morphological changes accompanying the initiation and progress of myelin production in the dorsal funiculus of the rat spinal cord , 1971, The Journal of comparative neurology.

[4]  Heidi Johansen-Berg,et al.  Motor Skill Learning Induces Changes in White Matter Microstructure and Myelination , 2013, The Journal of Neuroscience.

[5]  P. Stys,et al.  The molecular physiology of the axo-myelinic synapse , 2016, Experimental Neurology.

[6]  D. Attwell,et al.  Endogenous GABA controls oligodendrocyte lineage cell number, myelination, and CNS internode length , 2016, Glia.

[7]  John H. Martin,et al.  Electrical stimulation of the medullary pyramid promotes proliferation and differentiation of oligodendrocyte progenitor cells in the corticospinal tract of the adult rat , 2010, Neuroscience Letters.

[8]  R. Douglas Fields,et al.  Control of Local Protein Synthesis and Initial Events in Myelination by Action Potentials , 2011, Science.

[9]  H. Johansen-Berg,et al.  Unraveling the secrets of white matter – Bridging the gap between cellular, animal and human imaging studies , 2014, Neuroscience.

[10]  T. Kishimoto,et al.  Environmental enrichment stimulates progenitor cell proliferation in the amygdala , 2009, Journal of neuroscience research.

[11]  F. Nicoletti,et al.  Glial metabotropic glutamate receptor-4 increases maturation and survival of oligodendrocytes , 2015, Front. Cell. Neurosci..

[12]  Daniel J. Miller,et al.  Prolonged myelination in human neocortical evolution , 2012, Proceedings of the National Academy of Sciences.

[13]  S. Löwel,et al.  Oligodendroglial NMDA Receptors Regulate Glucose Import and Axonal Energy Metabolism , 2016, Neuron.

[14]  Samuel Bernard,et al.  Dynamics of Oligodendrocyte Generation and Myelination in the Human Brain , 2014, Cell.

[15]  James L. Sinclair,et al.  Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing , 2015, Nature Communications.

[16]  D. Attwell,et al.  NMDA receptors are expressed in oligodendrocytes and activated in ischaemia , 2005, Nature.

[17]  R. Káradóttir,et al.  Glutamate signalling: A multifaceted modulator of oligodendrocyte lineage cells in health and disease , 2016, Neuropharmacology.

[18]  D. Katz,et al.  Cellular Mechanisms Regulating Activity-Dependent Release of Native Brain-Derived Neurotrophic Factor from Hippocampal Neurons , 2002, The Journal of Neuroscience.

[19]  J. Maisin,et al.  A glial progenitor cell in the cerebral cortex of the adult rat , 1986, Journal of neurocytology.

[20]  J. Frahm,et al.  Elevated Phosphatidylinositol 3,4,5-Trisphosphate in Glia Triggers Cell-Autonomous Membrane Wrapping and Myelination , 2010, The Journal of Neuroscience.

[21]  R. Fields,et al.  Control of Myelination by Specific Patterns of Neural Impulses , 1998, The Journal of Neuroscience.

[22]  P. Somogyi,et al.  Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus , 2000, Nature.

[23]  B. Barres,et al.  Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons , 1993, Nature.

[24]  E. Ullian,et al.  Dynamic Modulation of Myelination in Response to Visual Stimuli Alters Optic Nerve Conduction Velocity , 2016, The Journal of Neuroscience.

[25]  R. Colello,et al.  Signals that initiate myelination in the developing mammalian nervous system , 1997, Molecular Neurobiology.

[26]  T. Tsumoto,et al.  Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Jens Frahm,et al.  Dysregulated expression of neuregulin-1 by cortical pyramidal neurons disrupts synaptic plasticity. , 2014, Cell reports.

[28]  T. Südhof,et al.  Neurotransmitter Release: The Last Millisecond in the Life of a Synaptic Vesicle , 2013, Neuron.

[29]  V. Gallo,et al.  NG2‐positive cells in the mouse white and grey matter display distinct physiological properties , 2004, The Journal of physiology.

[30]  Michelle K. Leach,et al.  A culture system to study oligodendrocyte myelination-processes using engineered nanofibers , 2012, Nature Methods.

[31]  S. Hayasaka,et al.  Quantitative study of the development of the optic nerve in rats reared in the dark during early postnatal life. , 1991, Journal of anatomy.

[32]  D. Attwell,et al.  Node of Ranvier length as a potential regulator of myelinated axon conduction speed , 2017, eLife.

[33]  W. Richardson,et al.  Rapid production of new oligodendrocytes is required in the earliest stages of motor skill learning , 2016, Nature Neuroscience.

[34]  D. Bergles,et al.  Vesicular release of glutamate from unmyelinated axons in white matter , 2007, Nature Neuroscience.

[35]  E. Schuman,et al.  Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus , 1995, Science.

[36]  Roberto Malinow,et al.  The Neuregulin-1 Receptor ErbB4 Controls Glutamatergic Synapse Maturation and Plasticity , 2007, Neuron.

[37]  D. Kirschner,et al.  Constitutively Active Akt Induces Enhanced Myelination in the CNS , 2008, The Journal of Neuroscience.

[38]  M. Descheˆnes,et al.  Axonal branch diameter and spacing of nodes in the terminal arborization of identified thalamic and cortical neurons , 1980, Brain Research.

[39]  K. Nave,et al.  Myelination and oligodendrocyte functions in psychiatric diseases. , 2014, JAMA psychiatry.

[40]  G. Corfas,et al.  Dynamic regulation of myelination in health and disease. , 2014, JAMA psychiatry.

[41]  William D. Richardson,et al.  Motor skill learning requires active central myelination , 2014, Science.

[42]  C. ffrench-Constant,et al.  Individual Oligodendrocytes Have Only a Few Hours in which to Generate New Myelin Sheaths In Vivo , 2013, Developmental cell.

[43]  B. Trapp,et al.  NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia , 2006, Nature.

[44]  M. Schachner,et al.  Antibodies to the L1 adhesion molecule inhibit Schwann cell ensheathment of neurons in vitro , 1989, The Journal of cell biology.

[45]  M. Kukley,et al.  Vesicular glutamate release from axons in white matter , 2007, Nature Neuroscience.

[46]  F. Tilney,et al.  MYELINOGENY AS APPLIED TO THE STUDY OF BEHAVIOR , 1924 .

[47]  T. Hashikawa,et al.  Protein processing and releases of neuregulin‐1 are regulated in an activity‐dependent manner , 2004, Journal of neurochemistry.

[48]  G. Turrigiano.  Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. , 2011, Annual review of neuroscience.

[49]  C. Hildebrand,et al.  Changing relation between onset of myelination and axon diameter range in developing feline white matter , 1982, Journal of the Neurological Sciences.

[50]  D. Attwell,et al.  Neuregulin and BDNF Induce a Switch to NMDA Receptor-Dependent Myelination by Oligodendrocytes , 2013, PLoS biology.

[51]  Y. Assaf,et al.  Diffusion MRI of Structural Brain Plasticity Induced by a Learning and Memory Task , 2011, PloS one.

[52]  R. Sturrock.  MYELINATION OF THE MOUSE CORPUS CALLOSUM , 1980, Neuropathology and applied neurobiology.

[53]  J. Chan,et al.  The geometric and spatial constraints of the microenvironment induce oligodendrocyte differentiation , 2008, Proceedings of the National Academy of Sciences.

[54]  Mark H. Johnson,et al.  Mapping Infant Brain Myelination with Magnetic Resonance Imaging , 2011, The Journal of Neuroscience.

[55]  Martin P. Meyer,et al.  Explorer Individual Neuronal Subtypes Exhibit Diversity in CNS Myelination Mediated by Synaptic Vesicle Release , 2016 .

[56]  G. Corfas,et al.  A Critical Period for Social Experience–Dependent Oligodendrocyte Maturation and Myelination , 2012, Science.

[57]  M. Luyckx,et al.  [Excitatory amino acid receptors]. , 1991, Journal de pharmacie de Belgique.

[58]  Li I. Zhang,et al.  Electrical activity and development of neural circuits , 2001, Nature Neuroscience.

[59]  R. Fields,et al.  White matter in learning, cognition and psychiatric disorders , 2008, Trends in Neurosciences.

[60]  H. Persson,et al.  Myelinated nerve fibres in the CNS , 1993, Progress in Neurobiology.

[61]  A. MacKay,et al.  How does magnetization transfer influence mcDESPOT results? , 2015, Magnetic resonance in medicine.

[62]  V. Gallo,et al.  Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

[64]  Kylie H. Alm,et al.  Development of the uncinate fasciculus: Implications for theory and developmental disorders , 2015, Developmental Cognitive Neuroscience.

[65]  Philip Chu,et al.  Organization of myelin in the mouse somatosensory barrel cortex and the effects of sensory deprivation , 2013, Developmental neurobiology.

[66]  Peter B. Jones,et al.  373. Adolescence is Associated with Genomically Patterned Consolidation of the Hubs of the Human Brain Connectome , 2016, Biological Psychiatry.

[67]  E. J. Lang,et al.  Role of myelination in the development of a uniform olivocerebellar conduction time. , 2003, Journal of neurophysiology.

[68]  K. Nave,et al.  Myelin Membrane Wrapping of CNS Axons by PI(3,4,5)P3-Dependent Polarized Growth at the Inner Tongue , 2014, Cell.

[69]  T. Malmfors,et al.  Myelinization of the optic nerve and its dependence on visual function--a quantitative investigation in mice. , 1963, Journal of embryology and experimental morphology.

[70]  R. Reynolds,et al.  Neuronal activity regulates remyelination via glutamate signalling to oligodendrocyte progenitors , 2015, Nature Communications.

[71]  Li Jiang,et al.  Type III Neuregulin 1 Is Required for Multiple Forms of Excitatory Synaptic Plasticity of Mouse Cortico-Amygdala Circuits , 2013, The Journal of Neuroscience.

[72]  M. Götz,et al.  Progenitors in the adult cerebral cortex: Cell cycle properties and regulation by physiological stimuli and injury , 2011, Glia.

[73]  Stefan Skare,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Extensive Blockinpiano Blockinpracticing Blockinhas Blockinregionally Specific Blockineffects Blockinon Blockinwhite Blockinmatter Blockindevelopment , 2022 .

[74]  V. Neuhoff,et al.  Myelination in rabbit optic nerves is accelerated by artificial eye opening , 1980, Neuroscience Letters.

[75]  F. Vaccarino,et al.  Excitatory amino acid receptors in glial progenitor cells: Molecular and functional properties , 1994, Glia.

[76]  D. Attwell,et al.  Oligodendrocyte Dynamics in the Healthy Adult CNS: Evidence for Myelin Remodeling , 2013, Neuron.

[77]  H. Kinney,et al.  Sequence of Central Nervous System Myelination in Human Infancy. II. Patterns of Myelination in Autopsied Infants , 1988, Journal of neuropathology and experimental neurology.

[78]  Ethan K. Scott,et al.  Neuronal activity biases axon selection for myelination in vivo , 2015, Nature Neuroscience.

[79]  C. ffrench-Constant,et al.  CNS Myelin Sheath Lengths Are an Intrinsic Property of Oligodendrocytes , 2015, Current Biology.

[80]  D. Attwell,et al.  Signalling through AMPA receptors on oligodendrocyte precursors promotes myelination by enhancing oligodendrocyte survival , 2017, eLife.

[81]  R. Fields,et al.  Regulated Expression of the Neural Cell Adhesion Molecule L1 by Specific Patterns of Neural Impulses , 1995, Science.

[82]  Edwin W Rubel,et al.  Differential Conduction Velocity Regulation in Ipsilateral and Contralateral Collaterals Innervating Brainstem Coincidence Detector Neurons , 2014, The Journal of Neuroscience.

[83]  P. Shrager,et al.  Control of myelination, axonal growth, and synapse formation in spinal cord explants by ion channels and electrical activity. , 1995, Brain research. Developmental brain research.

[84]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

[85]  M. Seghier,et al.  An anatomical signature for literacy , 2009, Nature.

[86]  Kenneth J. Smith,et al.  Axonal morphological changes following impulse activity in mouse peripheral nerve in vivo: the return pathway for sodium ions , 2015, The Journal of physiology.

[87]  B. Lu,et al.  Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus , 1996, Nature.

[88]  J. Lübke,et al.  The principal neurons of the medial nucleus of the trapezoid body and NG2+ glial cells receive coordinated excitatory synaptic input , 2009, The Journal of general physiology.

[89]  V. Gallo,et al.  Satellite NG2 Progenitor Cells Share Common Glutamatergic Inputs with Associated Interneurons in the Mouse Dentate Gyrus , 2008, The Journal of Neuroscience.

[90]  M. Fukaya,et al.  Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain , 2013, Nature Neuroscience.

[91]  J. Frisén,et al.  Why Adults Need New Brain Cells , 2013, Science.

[92]  Yaniv Assaf,et al.  Short-Term Learning Induces White Matter Plasticity in the Fornix , 2013, The Journal of Neuroscience.

[93]  Yasuyuki Taki,et al.  White matter structures associated with creativity: Evidence from diffusion tensor imaging , 2010, NeuroImage.

[94]  Richard Reynolds,et al.  NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS , 2003, Molecular and Cellular Neuroscience.

[95]  N. Kessaris,et al.  PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice , 2008, Nature Neuroscience.

[96]  M. L. Pucak,et al.  NMDA Receptor Signaling in Oligodendrocyte Progenitors Is Not Required for Oligodendrogenesis and Myelination , 2011, The Journal of Neuroscience.

[97]  Armin H. Seidl,et al.  Systematic and differential myelination of axon collaterals in the mammalian auditory brainstem , 2016, Glia.

[98]  Katrin Amunts,et al.  White matter fiber tracts of the human brain: Three-dimensional mapping at microscopic resolution, topography and intersubject variability , 2006, NeuroImage.

[99]  Bimal Lakhani,et al.  Motor Skill Acquisition Promotes Human Brain Myelin Plasticity , 2016, Neural plasticity.

[100]  S. Duan,et al.  Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons , 2010, Nature Neuroscience.

[101]  Wei Wu,et al.  Real-Time CARS Imaging Reveals a Calpain-Dependent Pathway for Paranodal Myelin Retraction during High-Frequency Stimulation , 2011, PloS one.

[102]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[103]  Carmen Birchmeier,et al.  Neuregulin-1/ErbB Signaling Serves Distinct Functions in Myelination of the Peripheral and Central Nervous System , 2008, Neuron.

[104]  P. J. Basser,et al.  Role of myelin plasticity in oscillations and synchrony of neuronal activity , 2014, Neuroscience.

[105]  V. Gallo,et al.  A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. , 1998, Development.

[106]  Christopher W Mount,et al.  Neuronal Activity Promotes Oligodendrogenesis and Adaptive Myelination in the Mammalian Brain , 2014, Science.

[107]  R. Colello,et al.  The chronology of oligodendrocyte differentiation in the rat optic nerve: evidence for a signaling step initiating myelination in the CNS , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[108]  Dwight E Bergles,et al.  Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus , 2004, Nature Neuroscience.

[109]  B. Stankoff,et al.  Induction of myelination in the central nervous system by electrical activity. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[110]  Mary Kay Lobo,et al.  Impaired adult myelination in the prefrontal cortex of socially isolated mice , 2012, Nature Neuroscience.

[111]  M. Schachner,et al.  Inhibition of Schwann cell myelination in vitro by antibody to the L1 adhesion molecule , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[112]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[113]  M. Schachner,et al.  Axonal cell-adhesion molecule L1 in CNS myelination. , 2004, Neuron glia biology.

[114]  S. Nelson,et al.  Distinct Profiles of Myelin Distribution Along Single Axons of Pyramidal Neurons in the Neocortex , 2014 .

[115]  D. Fulton,et al.  Neuronal activity and AMPA‐type glutamate receptor activation regulates the morphological development of oligodendrocyte precursor cells , 2015, Glia.

[116]  J. Chan,et al.  A rapid and reproducible assay for modeling myelination by oligodendrocytes using engineered nanofibers , 2013, Nature Protocols.